Ancient cis-regulatory constraints and the evolution of genome architecture

Trends in Genetics

Volumn 29, Issue 9, 2013, Pages 521-528

  Irimia, Manuel ^a   Maeso, Ignacio ^b   Roy, Scott W ^c   Fraser, Hunter B ^d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c SAN FRANCISCO STATE UNIVERSITY   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Cis regulatory element; Genome evolution; Synteny

Indexed keywords

ANIMAL; BYSTANDER EFFECT; CHROMOSOME; CIS REGULATORY ELEMENT; DEVELOPMENTAL GENE; GENE ORDER; GENE STRUCTURE; GENETIC ASSOCIATION; GENOME; MEDICAL RESEARCH; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNTENY; TRANSCRIPTION REGULATION;

EUKARYOTA; METAZOA;

EID: 84882611819     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2013.05.008     Document Type: Review

References (93)

1. Nadeau J.H., Taylor B.A. Lengths of chromosomal segments conserved since divergence of man and mouse. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:814-818.
2. Bulger M., et al. Conservation of sequence and structure flanking the mouse and human beta-globin loci: the beta-globin genes are embedded within an array of odorant receptor genes. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:5129-5134.
3. Spitz F., et al. Inversion-induced disruption of the Hoxd cluster leads to the partition of regulatory landscapes. Nat. Genet. 2005, 37:889-893.
4. Montavon T., et al. A regulatory archipelago controls Hox genes transcription in digits. Cell 2011, 147:1132-1145.
5. Filion G.J., et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 2010, 143:212-224.
6. Lee B.K., Iyer V.R. Genome-wide studies of CCCTC-binding factor (CTCF) and cohesin provide insight into chromatin structure and regulation. J. Biol. Chem. 2012, 287:30906-30913.
7. Nelson C., et al. The regulatory content of intergenic DNA shapes genome architecture. Genome Biol. 2004, 5:R25.
8. Nobrega M.A., et al. Scanning human gene deserts for long-range enhancers. Science 2003, 302:413.
9. Woolfe A., et al. Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol. 2005, 3:e7.
10. Engstrom P.G., et al. Genomic regulatory blocks underlie extensive microsynteny conservation in insects. Genome Res. 2007, 17:1898-1908.
11. Kikuta H., et al. Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res. 2007, 17:545-555.
12. Vavouri T., Lehner B. Conserved noncoding elements and the evolution of animal body plans. Bioessays 2009, 31:727-735.
13. Srivastava M., et al. The Trichoplax genome and the nature of placozoans. Nature 2008, 454:955-960.
14. Srivastava M., et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720-726.
15. Putnam N., et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 2008, 453:1064-1071.
16. Putnam N.H., et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86-94.
17. Maeso I., et al. An ancient genomic regulatory block conserved across bilaterians and its dismantling in tetrapods by retrogene replacement. Genome Res. 2012, 22:642-655.
18. Irimia M., et al. Comparative genomics of the Hedgehog loci in chordates and the origins of Shh regulatory novelties. Sci. Rep. 2012, 2:433.
19. Wang W., et al. Comparison of Pax1/9 locus reveals 500-Myr-old syntenic block and evolutionary conserved noncoding regions. Mol. Biol. Evol. 2007, 24:784-791.
20. Royo J.L., et al. Transphyletic conservation of developmental regulatory state in animal evolution. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14186-14191.
21. Clarke S.L., et al. Human developmental enhancers conserved between deuterostomes and protostomes. PLoS Genet. 2012, 8:e1002852.
22. Simakov O., et al. Insights into bilaterian evolution from three spiralian genomes. Nature 2013, 493:526-531.
23. Lv J., et al. Constraints on genes shape long-term conservation of macro-synteny in metazoan genomes. BMC Bioinformatics 2011, 12:S11.
24. Irimia M., et al. Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res. 2012, 22:2356-2367.
25. Akalin A., et al. Transcriptional features of genomic regulatory blocks. Genome Biol. 2009, 10:R38.
26. Birnbaum R.Y., et al. Coding exons function as tissue-specific enhancers of nearby genes. Genome Res. 2012, 22:1059-1068.
27. Perry M.W., et al. Shadow enhancers foster robustness of Drosophila gastrulation. Curr. Biol. 2010, 20:1562-1567.
28. Frankel N., et al. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 2010, 466:490-493.
29. Schmidt D., et al. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 2010, 328:1036-1040.
30. Schmidt D., et al. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 2012, 148:335-348.
31. Hong J.W., et al. Shadow enhancers as a source of evolutionary novelty. Science 2008, 321:1314.
32. Jeong Y., et al. A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers. Development 2006, 133:761-772.
33. Sahagun V., Ranz J.M. Characterization of genomic regulatory domains conserved across the genus Drosophila. Genome Biol. Evol. 2012, 4:1054-1060.
34. von Grotthuss M., et al. Fragile regions and not functional constraints predominate in shaping gene organization in the genus Drosophila. Genome Res. 2010, 20:1084-1096.
35. Lettice L.A., et al. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 2003, 12:1725-1735.
36. Seo H.C., et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 2004, 431:67-71.
37. Goode D.K., et al. Minor change, major difference: divergent functions of highly conserved cis-regulatory elements subsequent to whole genome duplication events. Development 2011, 138:879-884.
38. Cañestro C., et al. Impact of gene gains, losses and duplication modes on the origin and diversification of vertebrates. Semin. Cell Dev. Biol. 2013, 24:83-94.
39. Fukuoka Y., et al. Inter-species differences of co-expression of neighboring genes in eukaryotic genomes. BMC Genomics 2004, 5:4.
40. Hurst L.D., et al. The evolutionary dynamics of eukaryotic gene order. Nat. Rev. Genet. 2004, 5:299-310.
41. Stoltzfus A. On the possibility of constructive neutral evolution. J. Mol. Evol. 1999, 49:169-181.
42. Gray M.W., et al. Irremediable complexity?. Science 2010, 330:920-921.
43. Kim T.K., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
44. Djebali S., et al. Landscape of transcription in human cells. Nature 2012, 489:101-108.
45. Katayama S., et al. Antisense transcription in the mammalian transcriptome. Science 2005, 309:1564-1566.
46. Morrissy A.S., et al. Extensive relationship between antisense transcription and alternative splicing in the human genome. Genome Res. 2011, 21:1203-1212.
47. Ernst J., et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473:43-49.
48. de Almeida S.F., et al. Splicing enhances recruitment of methyltransferase HYPB/Setd2 and methylation of histone H3 Lys36. Nat. Struct. Mol. Biol. 2011, 18:977-983.
49. Imai K.S., et al. Cis-acting transcriptional repression establishes a sharp boundary in chordate embryos. Science 2012, 337:964-967.
50. Wang K.C., et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 2011, 472:120-124.
51. Thurman R.E., et al. The accessible chromatin landscape of the human genome. Nature 2012, 489:75-82.
52. Ghisletti S., et al. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 2010, 32:317-328.
53. Bogdanović O., et al. Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis. Genome Res. 2012, 22:2043-2053.
54. Visel A., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
55. Giles N.H., et al. The Wilhelmine E. Key 1989 invitational lecture. Organization and regulation of the qa (quinic acid) genes in Neurospora crassa and other fungi. J. Hered. 1991, 82:1-7.
56. Dean R.A., et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
57. Guyot R., et al. Ancestral synteny shared between distantly-related plant species from the asterid (Coffea canephora and Solanum Sp.) and rosid (Vitis vinifera) clades. BMC Genomics 2012, 13:103.
58. Merchan F., et al. Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol. 2009, 10:R136.
59. Lescot M., et al. Insights into the Musa genome: syntenic relationships to rice and between Musa species. BMC Genomics 2008, 9:58.
60. Dávila López M., et al. Computational screen for spliceosomal RNA genes aids in defining the phylogenetic distribution of major and minor spliceosomal components. Nucleic Acids Res. 2008, 36:3001-3010.
61. Kaufmann K., et al. Regulation of transcription in plants: mechanisms controlling developmental switches. Nat. Rev. Genet. 2010, 11:830-842.
62. Baxter L., et al. Conserved noncoding sequences highlight shared components of regulatory networks in dicotyledonous plants. Plant Cell 2012, 24:3949-3965.
63. Kritsas K., et al. Computational analysis and characterization of UCE-like elements (ULEs) in plant genomes. Genome Res. 2012, 22:2455-2466.
64. Causier B., et al. Conserved intragenic elements were critical for the evolution of the floral C-function. Plant J. 2009, 58:41-52.
65. Stam M., et al. The regulatory regions required for B' paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics 2002, 162:917-930.
66. Clark R.M., et al. A distant upstream enhancer at the maize domestication gene tb0010 has pleiotropic effects on plant and inflorescent architecture. Nat. Genet. 2006, 38:594-597.
67. Heger P., et al. The chromatin insulator CTCF and the emergence of metazoan diversity. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:17507-17512.
68. Kruse K., et al. A complex network framework for unbiased statistical analyses of DNA-DNA contact maps. Nucleic Acids Res. 2013, 41:701-710.
69. Parelho V., et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132:422-433.
70. Nasmyth K., Haering C.H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 2009, 43:525-558.
71. Finan K., et al. Non-specific (entropic) forces as major determinants of the structure of mammalian chromosomes. Chromosome Res. 2011, 19:53-61.
72. Martín-Durán J.M., et al. Deuterostomic development in the protostome Priapulus caudatus. Curr. Biol. 2012, 22:2161-2166.
73. Halanych K.M., et al. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 1995, 267:1641-1643.
74. Aguinaldo A.M.A., et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 1997, 387:489-493.
75. Becker T.S., Lenhard B. The random versus fragile breakage models of chromosome evolution: a matter of resolution. Mol. Genet. Genomics 2007, 278:487-491.
76. Chibana H., et al. Sequence finishing and gene mapping for Candida albicans chromosome 7 and syntenic analysis against the Saccharomyces cerevisiae genome. Genetics 2005, 170:1525-1537.
77. Espagne E., et al. The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol. 2008, 9:R77.
78. Borkovich K.A., et al. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 2004, 68:1-108.
79. Galagan J.E., et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 2005, 438:1105-1115.
80. Machida M., et al. Genome sequencing and analysis of Aspergillus oryzae. Nature 2005, 438:1157-1161.
81. Hane J.K., et al. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol. 2011, 12:R45.
82. Ming R., et al. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 2008, 452:991-996.
83. Tang H., et al. Synteny and collinearity in plant genomes. Science 2008, 320:486-488.
84. Jung S., et al. Comparative genomic sequence analysis of strawberry and other rosids reveals significant microsynteny. BMC Res. Notes 2010, 3:168.
85. Jung S., et al. Synteny of Prunus and other model plant species. BMC Genomics 2009, 10:76.
86. Initiative I.B. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463:763-768.
87. Murat F., et al. Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. Genome Res. 2010, 20:1545-1557.
88. Tang H., et al. Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:472-477.
89. Fawcett J.A., et al. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5737-5742.
90. Banks J.A., et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 2011, 332:960-963.
91. Zuccolo A., et al. A physical map for the Amborella trichopoda genome sheds light on the evolution of angiosperm genome structure. Genome Biol. 2011, 12:R48.
92. Lévesque C.A., et al. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol. 2010, 11:R73.
93. Ohm R.A., et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen dothideomycetes fungi. PLoS Pathog. 2012, 8:e1003037.